A new selective developmental deficit: Impaired object recognition with normal face recognition

Introduction

Studies of developmental deficits in face recognition, or developmental prosopagnosia, have shown that individuals who have not suffered brain damage can show face recognition impairments coupled with normal object recognition ( [Duchaine and Nakayama, 2005] , [Duchaine et?al., 2006] and [Nunn et?al., 2001] ). However, no developmental cases with the opposite dissociation – normal face recognition with impaired object recognition – have been reported. The existence of a case of non-face developmental visual agnosia would indicate that the development of normal face recognition mechanisms does not rely on the development of normal object recognition mechanisms.

Methods

To see whether a developmental variant of non-face visual object agnosia exists, we conducted a series of web-based object and face recognition tests to screen for individuals showing object recognition memory impairments but not face recognition impairments. Through this screening process, we identified AW, an otherwise normal 19-year-old female, who was then tested in the lab on face and object recognition tests.

Results

AW’s performance was impaired in within-class visual recognition memory across six different visual categories (guns, horses, scenes, tools, doors, and cars). In contrast, she scored normally on seven tests of face recognition, tests of memory for two other object categories (houses and glasses), and tests of recall memory for visual shapes. Testing confirmed that her impairment was not related to a general deficit in lower-level perception, object perception, basic-level recognition, or memory.

Discussion

AW’s results provide the first neuropsychological evidence that recognition memory for non-face visual object categories can be selectively impaired in individuals without brain damage or other memory impairment. These results indicate that the development of recognition memory for faces does not depend on intact object recognition memory and provide further evidence for category-specific dissociations in visual recognition.     

Disorders of face perception and recognition

Face recognition is one of the most complex visual tasks performed by the human brain. Data from monkeys suggest that area IT may play a key role in identifying faces, and functional imaging research suggests that the human homologue of IT may be located in the medial occipitotemporal cortex, where a FFA has been located. Damage to medial occipitotemporal structures on the right or bilaterally leads to prosopagnosia, the failure to recognize facial identity. Prosopagnosia is not a single functional disorder but a family of dysfunctions, with different patients having different degrees of impairments to various perceptual and memory stages involved in face processing. Understanding the perceptual basis of this disorder and epiphenomena, such as covert recognition, is a goal of current research. Deficits in face perception also may contribute to Capgras syndrome and may be related to the impaired social development of patients with Asperger syndrome. More recently, identified deficits in face processing include the false recognition of unfamiliar faces and the impaired extraction of social information from faces, independent of the recognition of identity. Many of these prosopagnosia and other face processing deficits can be placed in the context of cognitive models of face processing stages, which are being refined continually by data from neurologic patients and functional imaging in normal subjects.     

Covert recognition in acquired and developmental prosopagnosia

BACKGROUND: Some patients with prosopagnosia have covert recognition, meaning that they retain some familiarity or knowledge of facial identity of which they are not aware. OBJECTIVE:To test the hypothesis that prosopagnosic patients with right occipitotemporal lesions and impaired face perception lack covert processing, whereas patients with associative prosopagnosia and bilateral anterior temporal lesions possess it. METHODS: Eight patients with prosopagnosia were tested with a battery of four face recognition tests to determine their ability to discriminate between famous and unknown faces. RESULTS: Measures of overt familiarity revealed better residual discrimination in patients with acquired prosopagnosia than in those with the developmental form. With forced-choice methods using famous faces paired with unknown faces, no patient demonstrated covert familiarity. However, when the semantic cue of the name of the famous face was provided, covert processing was present in all five patients with acquired prosopagnosia, including the three with extensive right-sided lesions and impaired perceptual discrimination of facial configuration. Sorting unrecognized faces by occupation was also performed above chance in three of these five patients. In contrast, none of the three patients with developmental prosopagnosia had covert processing, even though two demonstrated flawless performance on similar tests of name (rather than face) recognition. Overt familiarity correlated highly with the degree of covert recognition. CONCLUSIONS: Extensive right occipitotemporal lesions with significant deficits in face perception are not incompatible with covert face processing. Covert processing is absent in developmental prosopagnosia, because this condition likely precludes the establishment of a store of accurate facial memories. The presence of covert processing correlates with the degree of residual overt familiarity, indicating that these are related phenomena.     

Normal and abnormal face selectivity of the M170 response in developmental prosopagnosics

Developmental prosopagnosia is a lifelong impairment in face recognition despite normal low-level visual processing. Here we used magnetoencephalography (MEG) to examine the M170 response, a component occurring approximately 170 ms after stimulus onset, in a group of five developmental prosopagnosics. In normal subjects, the M170 is “face-selective”, with a consistently higher amplitude to faces than to a wide variety of other visual stimulus categories; the N170, a component recorded using event-related potentials (ERP) and thought to be analogous to the M170, also shows this “face selectivity”. Two previous ERP studies with developmental prosopagnosics have found attenuation or absence of face selectivity in the N170 response of these subjects [Bentin, S., Deouell, L. Y., & Soroker, N. (1999). Selective visual streaming in face recognition: Evidence from developmental prosopagnosia. Neuroreport, 10, 823–827; Kress, T., & Daum, I. (2003). Event-related potentials reflect impaired face recognition in patients with congenital prosopagnosia. Neuroscience Letters, 352, 133–136]. Three of our developmental prosopagnosic group showed this non-selective pattern at the M170 while the remaining two prosopagnosics were indistinguishable from normal controls. Thus, impaired face recognition is not necessarily correlated with an absence of the “face-selective” M170. Furthermore, ERP recordings collected simultaneously in the two developmental prosopagnosics with seemingly selective M170s also showed N170s within the same normal selective range, demonstrating that the face-selective signals found with MEG are not due to differences between MEG and ERP. While the presence of face selectivity at these neurophysiological markers is insufficient for predicting normal behavioral performance with faces, it could help to distinguish different classes of face recognition deficits.     

Prevalence and correlates of face recognition impairments after acquired brain injury

Impairments of face recognition after acquired brain injury (ABI) are not restricted to prosopagnosia but commonly arise in association with other cognitive deficits and can be psychosocially debilitating. Despite this, the prevalence and cognitive concomitants of such impairments after ABI have not been systematically investigated. We tested 91 adults with ABI on a range of cognitive measures including several indices of face recognition and learning. The proportion of patients who show impaired performance varied across face learning/recognition tests between 21% and 80%. Principal components analyses indicated orthogonality between impairments of "directed facial processing", associated with memory and visuoperceptual deficits and manifest in slow learning and matching of previously unfamiliar faces, and of "face identification", associated with deficits on verbal tests and manifest in difficulty in naming famous faces. Theoretical and rehabilitative implications are considered.     

Prevalence and correlates of face recognition impairments after acquired brain injury

Impairments of face recognition after acquired brain injury (ABI) are not restricted to prosopagnosia but commonly arise in association with other cognitive deficits and can be psychosocially debilitating. Despite this, the prevalence and cognitive concomitants of such impairments after ABI have not been systematically investigated. We tested 91 adults with ABI on a range of cognitive measures including several indices of face recognition and learning. The proportion of patients who show impaired performance varied across face learning/recognition tests between 21% and 80%. Principal components analyses indicated orthogonality between impairments of “directed facial processing”, associated with memory and visuoperceptual deficits and manifest in slow learning and matching of previously unfamiliar faces, and of “face identification”, associated with deficits on verbal tests and manifest in difficulty in naming famous faces. Theoretical and rehabilitative implications are considered.     

Whole not hole: Expert face recognition requires holistic perception

Face recognition is an important ability of the human brain, yet its underlying mechanisms are still poorly understood. Two opposite views have been proposed to account for human face recognition expertise: the ability to extract the most diagnostic local information, feature-by feature (analytical view), or the ability to process all features at once over the whole face (holistic view). To help clarifying this debate, we used an original gaze-contingent stimulus presentation method to compare normal observers and a brain-damaged patient specifically impaired at face recognition (prosopagnosia). When a single central facial feature was revealed at a time through a gaze-contingent window, normal observers’ performance at an individual face matching task decreased to the patient level. However, when only the central feature was masked, forcing normal observers to rely on the whole face but the fixated feature, their performance was almost not affected. In contrast, the prosopagnosic patient's performance decreased dramatically in this latter condition. These results were independent of the absolute size of the face and window/mask. This dissociation indicates that expertise in face recognition does not rest on the ability to analyze diagnostic local detailed features sequentially but rather on the ability to see the individual features of a face all at once, a function that is critically impaired in acquired prosopagnosia.     

Visual search strategies during facial recognition in children with ASD

Facial recognition is a complex skill necessary for successful human interpersonal and social interactions. Given that the most prevalent disorder of social interaction is autism spectrum disorder (ASD), a number of studies have investigated and found impaired facial recognition abilities in people with ASD. Further, this impairment may be critically involved in mediating the deficits in interpersonal and social interactions in people with ASD. We sought to address the question of whether face processing is impaired in children with ASD in the current study. While there were a number of differences in visual search behaviours between the 19 children with ASD and the 15 controls, this did not manifest in deficits in facial recognition accuracy. In addition, there were notable differences with respect to eye fixation behaviours and recognition accuracy in this study compared to the findings in a previous similar study conducted in adults with ASD. These differences suggest a performance enhancing developmental trajectory in facial processing in controls that may not be present in individuals with ASD.     

“A room full of strangers every day”: The psychosocial impact of developmental prosopagnosia on children and their families

Objective

Individuals with developmental prosopagnosia (‘face blindness’) have severe face recognition difficulties due to a failure to develop the necessary visual mechanisms for recognizing faces. These difficulties occur in the absence of brain damage and despite normal low-level vision and intellect. Adults with developmental prosopagnosia report serious personal and emotional consequences from their inability to recognize faces, but little is known about the psychosocial consequences in childhood. Given the importance of face recognition in daily life, and the potential for unique social consequences of impaired face recognition in childhood, we sought to evaluate the impact of developmental prosopagnosia on children and their families.

Methods

We conducted semi-structured interviews with 8 children with developmental prosopagnosia and their parents. A battery of face recognition tests was used to confirm the face recognition impairment reported by the parents of each child. We used thematic analysis to develop common themes among the psychosocial experiences of the children and their parents.

Results

Three themes were developed from the child reports: 1) awareness of their difficulties, 2) coping strategies, such as using non-facial cues to identify others, and 3) social implications, such as discomfort in, and avoidance of, social situations. These themes were paralleled by the parent reports and highlight the unique social and practical challenges associated with childhood developmental prosopagnosia.

Conclusion

Our findings indicate a need for increased awareness and treatment of developmental prosopagnosia to help these children manage their face recognition difficulties and to promote their social and emotional wellbeing.     

Impairment of holistic face perception following right occipito-temporal damage in prosopagnosia: converging evidence from gaze-contingency

Gaze-contingency is a method traditionally used to investigate the perceptual span in reading by selectively revealing/masking a portion of the visual field in real time. Introducing this approach in face perception research showed that the performance pattern of a brain-damaged patient with acquired prosopagnosia (PS) in a face matching task was reversed, as compared to normal observers: the patient showed almost no further decrease of performance when only one facial part (eye, mouth, nose, etc.) was available at a time (foveal window condition, forcing part-based analysis), but a very large impairment when the fixated part was selectively masked (mask condition, promoting holistic perception) ( [Van Belle et al., 2010a] and [Van Belle et al., 2010b] ). Here we tested the same manipulation in a recently reported case of pure prosopagnosia (GG) with unilateral right hemisphere damage (Busigny, Joubert, Felician, Ceccaldi, & Rossion, 2010). Contrary to normal observers, GG was also significantly more impaired with a mask than with a window, demonstrating impairment with holistic face perception. Together with our previous study, these observations support a generalized account of acquired prosopagnosia as a critical impairment of holistic (individual) face perception, implying that this function is a key element of normal human face recognition. Furthermore, the similar behavioral pattern of the two patients despite different lesion localizations supports a distributed network view of the neural face processing structures, suggesting that the key function of human face processing, namely holistic perception of individual faces, requires the activity of several brain areas of the right hemisphere and their mutual connectivity.     

Dissociations of face and object recognition in developmental prosopagnosia

Neuropsychological studies with patients suffering from prosopagnosia have provided the main evidence for the hypothesis that the recognition of faces and objects rely on distinct mechanisms. Yet doubts remain, and it has been argued that no case demonstrating an unequivocal dissociation between face and object recognition exists due in part to the lack of appropriate response time measurements (Gauthier et al., 1999). We tested seven developmental prosopagnosics to measure their accuracy and reaction times with multiple tests of face recognition and compared this with a larger battery of object recognition tests. For our systematic comparison, we used an old/new recognition memory paradigm involving memory tests for cars, tools, guns, horses, natural scenes, and houses in addition to two separate tests for faces. Developmental prosopagnosic subjects performed very poorly with the face memory tests as expected. Four of the seven prosopagnosics showed a very strong dissociation between the face and object tests. Systematic comparison of reaction time measurements for all tests indicates that the dissociations cannot be accounted for by differences in reaction times. Contrary to an account based on speed accuracy tradeoffs, prosopagnosics were systematically faster in nonface tests than in face tests. Thus, our findings demonstrate that face and nonface recognition can dissociate over a wide range of testing conditions. This is further support for the hypothesis that face and nonface recognition relies on separate mechanisms and that developmental prosopagnosia constitutes a disorder separate from developmental agnosia.     

Prosopagnosia associated with a left occipitotemporal lesion

Acquired prosopagnosia is usually associated with bilateral or right-sided lesions of the occipital or temporal lobes. In rare cases of prosopagnosia after left-sided lesions in left-handed subjects, it is attributed to a reversed hemispheric specialization for face processing. This study examines the face-processing functions of a left-handed prosopagnosic patient with a left-sided lesion affecting the region of the occipital face area and possibly the fusiform face area, to contrast his deficits with those of prosopagnosic patients with right-hemispheric lesions. Similar to those patients, he has a moderately severe reduction in familiarity judgments, is impaired in processing face configuration, and shares with some of those patients a greater failure to process eye than mouth information, indicating an altered pattern of facial saliency. He has a mild reduction in the identification of exemplars of non-face objects. Unlike those patients, he has better residual familiarity on a two-alternative forced-choice task and can processing facial configuration if given more time, indicating a reduction in efficiency rather than a severe limitation. He has more difficulty accessing semantic-biographic information from names. He has trouble with facial feature imagery but not imagery for global face shape. Thus this subject's deficits represent a combination of impaired familiarity and configuration processing (normally right-sided functions in right-handed subjects), and impaired feature processing and access to semantic-biographic information (normally left-sided functions). His prosopagnosia likely reflects partially anomalous rather than reversed lateralization of hemispheric perceptual functions.     

Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia.

BACKGROUND: Prosopagnosia, the inability to recognize faces, is associated with medial occipitotemporal lesions, especially on the right. Functional imaging has revealed a focal region in the right fusiform gyrus activated specifically during face perception. OBJECTIVE: The study attempted to determine whether lesions of this region were associated with defects in face perception in patients with prosopagnosia. METHODS: Five patients with acquired prosopagnosia were tested. They were asked to discriminate faces in which the spatial configuration of features had been altered. This was contrasted with their discrimination of changes in feature color, an alteration that does not affect spatial relations. RESULTS: All four patients whose lesions included the right fusiform face area were severely impaired in discriminating changes in the spatial position of features. The one patient with anterior bilateral lesions was normal in this perceptual ability. For three of the five patients, accuracy was normal for changes in eye color. When subjects knew that only changes in mouth position would be shown, performance improved markedly in two of the four patients who were impaired in the initial test. CONCLUSION: Perception of facial configuration is impaired in patients with prosopagnosia whose lesions involve the right fusiform gyrus. This deficit is especially manifest when attention must be distributed across numerous facial elements. It does not occur with more anterior bilateral temporal lesions. Loss of this ability may contribute to the recognition defect in some forms of prosopagnosia.     

Face and emotion processing in frontal variant frontotemporal dementia.

Lavenu et al. [Alzheimer Dis. Assoc. Disorder 5 (1999) 96] have shown that patients with frontotemporal dementia (FTD) show impaired recognition of facial expressions. It is not clear, however, whether these deficits arise from an impairment affecting face processing generally, emotion processing generally, or facial expression recognition alone. We address this issue by testing six patients with frontal variant frontotemporal dementia (fvFTD) on a series of face perception tasks (including facial identity and facial expression recognition), and a test of vocal emotion recognition. In general, the fvFTD participants showed impaired recognition of facial expressions in the context of preserved recognition of facial identity. In addition, however, deficits were also observed for the vocal emotion recognition task. These results are consistent with the idea that fvFTD affects the recognition of emotional signals from multiple modalities rather than facial expression processing alone. It is plausible that the emotion recognition impairments observed contribute to the abnormal social behaviour that is characteristic of this condition.     

A comparative case study of face recognition: The contribution of configural and part-based recognition systems, and their interaction

Understanding the interaction between the configural and part-based systems in face recognition is the major aim of this study. Specifically, we established whether configural representation of faces contribute to aspects of face recognition that depend on part-based processes, such as identifying inverted or fractured faces. Using face recognition tasks that require part-based or configural processing, we compared the results of CK—a man who has object agnosia and alexia [Moscovitch, M., Winocur, G., & Behrmann, M. (1997). What is special about face recognition? Nineteen experiments on a person with visual object agnosia and dyslexia but normal face recognition. Journal of Cognitive Neuroscience, 9(5), 555–604] but normal upright face recognition, to those of DC—a man who has prosopagnosia but normal object recognition. CK was normal at recognizing faces if configural processing was sufficient, but poor at recognizing faces that were modified so as to alter their gestalt, and require part-based processing (Moscovitch et al.). DC was impaired at recognizing upright faces and his performance declined in all tasks involving recognition of modified faces, including those that depend on part-based and on configural processing. Nevertheless, DC was normal on tasks involving perception of generic faces and face imagery. These results show that although configural face perception can proceed without part-based processing, the reverse is not the case. Our results suggest that the configural system is always necessary for face recognition, and appears to support what remains of face identification even in prosopagnosic people who have an intact part-based system.     

Deficits in face perception in the amnestic form of mild cognitive impairment

The fusiform gyrus is involved pathologically at an early stage of the amnestic form of mild cognitive impairment (aMCI), and is also known to be involved in the perceptual stage of face processing. We assessed face perception in patients with aMCI to determine if this cognitive skill was impaired. We compared 12 individuals (4 men) with aMCI and 12 age- and education-matched healthy controls on the ability to discriminate changes in the spatial configuration or color of the eyes or the mouth in faces. Patients with aMCI performed less quickly and accurately for all changes on trials with limited viewing duration. With unlimited duration, they could achieve normal perceptual accuracy for configural changes to the mouth, but remained impaired for changes to eye color or configuration. Patients with aMCI show deficits in face perception that are more pronounced for the highly salient ocular region, a pattern similar to that seen in acquired prosopagnosia. This form of perceptual impairment may be an early marker of additional cognitive deficits beyond memory in aMCI.     

Selective visual streaming in face recognition: evidence from developmental prosopagnosia

Computational considerations suggest that efficient face identification requires the categorization and exclusive streaming of previously encoded face visual primitives into a dedicated face recognition system. Unique evidence supporting this claim is provided by a rare case of developmental pure prosopagnosia with otherwise normal visual and cognitive functions. Despite his normal visual memory and ability to describe faces, he is extremely impaired in face recognition. An early event related brain potential (N170) that is normally elicited exclusively by human faces, showed no specificity in this person. MRI revealed a smaller then normal right temporal lobe. These data emphasize the indispensability of the early streaming process for face recognition.     

Neurological disease and facial recognition

To discuss the neurological basis of facial recognition, we present our case reports of impaired recognition and a review of previous literature. First, we present a case of infarction and discuss prosopagnosia, which has had a large impact on face recognition research. From a study of patient symptoms, we assume that prosopagnosia may be caused by unilateral right occipitotemporal lesion and right cerebral dominance of facial recognition. Further, circumscribed lesion and degenerative disease may also cause progressive prosopagnosia. Apperceptive prosopagnosia is observed in patients with posterior cortical atrophy (PCA), pathologically considered as Alzheimer's disease, and associative prosopagnosia in frontotemporal lobar degeneration (FTLD). Second, we discuss face recognition as part of communication. Patients with Parkinson disease show social cognitive impairments, such as difficulty in facial expression recognition and deficits in theory of mind as detected by the reading the mind in the eyes test. Pathological and functional imaging studies indicate that social cognitive impairment in Parkinson disease is possibly related to damages in the amygdalae and surrounding limbic system. The social cognitive deficits can be observed in the early stages of Parkinson disease, and even in the prodromal stage, for example, patients with rapid eye movement (REM) sleep behavior disorder (RBD) show impairment in facial expression recognition. Further, patients with myotonic dystrophy type 1 (DM 1), which is a multisystem disease that mainly affects the muscles, show social cognitive impairment similar to that of Parkinson disease. Our previous study showed that facial expression recognition impairment of DM 1 patients is associated with lesion in the amygdalae and insulae. Our study results indicate that behaviors and personality traits in DM 1 patients, which are revealed by social cognitive impairment, are attributable to dysfunction of the limbic system.     

Impaired integration of emotional faces and affective body context in a rare case of developmental visual agnosia

In the current study we examined the recognition of facial expressions embedded in emotionally expressive bodies in case LG, an individual with a rare form of developmental visual agnosia (DVA) who suffers from severe prosopagnosia. Neuropsychological testing demonstrated that LG's agnosia is characterized by profoundly impaired visual integration. Unlike individuals with typical developmental prosopagnosia who display specific difficulties with face identity (but typically not expression) recognition, LG was also impaired at recognizing isolated facial expressions. By contrast, he successfully recognized the expressions portrayed by faceless emotional bodies handling affective paraphernalia. When presented with contextualized faces in emotional bodies his ability to detect the emotion expressed by a face did not improve even if it was embedded in an emotionally-congruent body context. Furthermore, in contrast to controls, LG displayed an abnormal pattern of contextual influence from emotionally-incongruent bodies. The results are interpreted in the context of a general integration deficit in DVA, suggesting that impaired integration may extend from the level of the face to the level of the full person.